Value estimation and latent-state update-related neural activity during fear conditioning predict posttraumatic stress disorder symptom severity.

Allison M Letkiewicz, Amy L Cochran, Anthony A Privratsky, G Andrew James, Josh M Cisler
Author Information
  1. Allison M Letkiewicz: Department of Psychiatry and Behavioral Sciences, Northwestern University, 680 N. Lakeshore Drive, Suite 1520, Chicago, IL, 60611, USA. allison.letkiewicz@northwestern.edu. ORCID
  2. Amy L Cochran: Departments of Math and Population Health Sciences, University of Wisconsin, Madison, WI, USA.
  3. Anthony A Privratsky: Department of Psychiatry, Brain Imaging Research Center, University of Arkansas for Medical Sciences, Little Rock, AR, USA.
  4. G Andrew James: Department of Psychiatry, Brain Imaging Research Center, University of Arkansas for Medical Sciences, Little Rock, AR, USA.
  5. Josh M Cisler: Department of Psychiatry, University of Wisconsin, Madison, WI, USA.

Abstract

Learning theories of posttraumatic stress disorder (PTSD) purport that fear-learning processes, such as those that support fear acquisition and extinction, are impaired. Computational models designed to capture specific processes involved in fear learning have primarily assessed model-free, or trial-and-error, reinforcement learning (RL). Although previous studies indicated that aspects of model-free RL are disrupted among individuals with PTSD, research has yet to identify whether model-based RL, which is inferential and contextually driven, is impaired. Given empirical evidence of aberrant contextual modulation of fear in PTSD, the present study sought to identify whether model-based RL processes are altered during fear conditioning among women with interpersonal violence (IPV)-related PTSD (n = 85) using computational modeling. Model-free, hybrid, and model-based RL models were applied to skin conductance responses (SCR) collected during fear acquisition and extinction, and the model-based RL model was found to provide the best fit to the SCR data. Parameters from the model-based RL model were carried forward to neuroimaging analyses (voxel-wise and independent component analysis). Results revealed that reduced activity within visual processing regions during model-based updating uniquely predicted higher PTSD symptoms. Additionally, after controlling for model-based updating, greater value estimation encoding within the left frontoparietal network during fear acquisition and reduced value estimation encoding within the dorsomedial prefrontal cortex during fear extinction predicted greater PTSD symptoms. Results provide evidence of disrupted RL processes in women with assault-related PTSD, which may contribute to impaired fear and safety learning, and, furthermore, may relate to treatment response (e.g., poorer response to exposure therapy).

Keywords

References

  1. Curr Opin Neurobiol. 2014 Apr;25:85-92 [PMID: 24709605]
  2. Cereb Cortex. 2017 Apr 1;27(4):2652-2670 [PMID: 27130661]
  3. Psychol Rev. 2007 Jul;114(3):784-805 [PMID: 17638506]
  4. Nat Neurosci. 2012 Mar 11;15(5):786-91 [PMID: 22406551]
  5. Eur J Psychotraumatol. 2017 Oct 27;8(sup5):1353383 [PMID: 29075426]
  6. Nat Commun. 2015 Sep 22;6:8165 [PMID: 26391305]
  7. Neuropsychol Rev. 2006 Mar;16(1):17-42 [PMID: 16794878]
  8. PLoS Comput Biol. 2019 Sep 16;15(9):e1007331 [PMID: 31525176]
  9. Int J Psychophysiol. 2015 Dec;98(3 Pt 2):594-605 [PMID: 25462219]
  10. J Trauma Stress. 2009 Jun;22(3):227-35 [PMID: 19444884]
  11. Psychophysiology. 2013 Jan;50(1):15-22 [PMID: 23094650]
  12. Elife. 2018 Jan 09;7: [PMID: 29313489]
  13. Psychol Med. 2020 Jul;50(9):1442-1451 [PMID: 31258096]
  14. Neuron. 2012 Dec 6;76(5):998-1009 [PMID: 23217747]
  15. J Psychiatr Res. 2015 Apr;63:75-83 [PMID: 25769397]
  16. J Abnorm Psychol. 2016 Aug;125(6):777-787 [PMID: 27175984]
  17. J Anxiety Disord. 2013 Jan;27(1):33-46 [PMID: 23247200]
  18. Neuron. 2014 Feb 5;81(3):687-99 [PMID: 24507199]
  19. J Neurosci. 2014 May 28;34(22):7522-30 [PMID: 24872557]
  20. Clin Psychol Rev. 2014 Apr;34(3):249-55 [PMID: 24681171]
  21. Psychiatry Res. 2009 May 15;167(1-2):151-60 [PMID: 19345420]
  22. Behav Res Ther. 2005 Apr;43(4):533-51 [PMID: 15701362]
  23. Psychol Violence. 2013 Jul;3(3):273-287 [PMID: 25232484]
  24. Q J Exp Psychol B. 2004 Jul;57(3):193-243 [PMID: 15204108]
  25. Biol Psychiatry. 2002 Dec 1;52(11):1079-88 [PMID: 12460691]
  26. Biol Psychol. 2014 Dec;103:63-8 [PMID: 25148785]
  27. J Neurosci. 2016 Jan 27;36(4):1211-22 [PMID: 26818509]
  28. Arch Gen Psychiatry. 1998 Jul;55(7):626-32 [PMID: 9672053]
  29. Transl Psychiatry. 2020 Aug 15;10(1):287 [PMID: 32801342]
  30. Arch Gen Psychiatry. 2005 Jun;62(6):617-27 [PMID: 15939839]
  31. J Psychiatr Res. 2022 Jan;145:256-262 [PMID: 33199053]
  32. Am J Psychiatry. 2017 Feb 1;174(2):125-134 [PMID: 27794690]
  33. Eur J Neurosci. 2013 Mar;37(5):758-67 [PMID: 23278978]
  34. J Consult Clin Psychol. 2002 Aug;70(4):867-79 [PMID: 12182270]
  35. J Neurosci. 2014 Oct 1;34(40):13435-43 [PMID: 25274821]
  36. Biol Psychiatry. 2019 Apr 1;85(7):606-612 [PMID: 30449531]
  37. Neurosci Biobehav Rev. 2016 Jan;60:31-42 [PMID: 26519776]
  38. J Neurosci. 2011 Feb 16;31(7):2700-5 [PMID: 21325538]
  39. Nat Neurosci. 2011 Sep 11;14(10):1250-2 [PMID: 21909088]
  40. Depress Anxiety. 2010 Mar;27(3):244-51 [PMID: 20143428]
  41. J Neurosci. 2008 Mar 12;28(11):2745-52 [PMID: 18337404]
  42. J Psychiatr Res. 2018 Aug;103:83-90 [PMID: 29783079]
  43. Biol Psychol. 2013 Dec;94(3):490-7 [PMID: 24063955]
  44. J Trauma Stress. 2012 Feb;25(1):33-40 [PMID: 22354506]
  45. Brain. 2009 Nov;132(Pt 11):3002-10 [PMID: 19713281]
  46. Comput Biomed Res. 1996 Jun;29(3):162-73 [PMID: 8812068]
  47. Nat Neurosci. 2016 Mar;19(3):404-13 [PMID: 26906507]
  48. Int J Psychophysiol. 2020 Dec;158:86-95 [PMID: 33075428]
  49. Cogn Neuropsychiatry. 2017 Jan;22(1):1-16 [PMID: 27875926]
  50. Neuroimage. 2010 Jan 1;49(1):772-81 [PMID: 19682583]
  51. Int J Psychophysiol. 2015 Dec;98(3 Pt 2):584-93 [PMID: 26149734]
  52. Front Neurosci. 2013 Jul 19;7:116 [PMID: 23882174]
  53. Neuron. 2010 May 27;66(4):585-95 [PMID: 20510862]
  54. Biol Psychiatry Cogn Neurosci Neuroimaging. 2019 Apr;4(4):371-380 [PMID: 30343131]
  55. Neuropharmacology. 2012 Feb;62(2):695-704 [PMID: 21377482]
  56. J Affect Disord. 2012 Dec 1;141(1):11-21 [PMID: 22310036]
  57. J Neurosci. 2004 Feb 4;24(5):1129-35 [PMID: 14762131]
  58. Neuron. 2011 Mar 24;69(6):1204-15 [PMID: 21435563]
  59. Nat Neurosci. 2019 Mar;22(3):470-476 [PMID: 30664770]
  60. Psychol Assess. 2018 Mar;30(3):383-395 [PMID: 28493729]
  61. J Neurosci. 2007 Nov 21;27(47):12860-7 [PMID: 18032658]
  62. Int J Psychophysiol. 2010 Mar;75(3):349-56 [PMID: 20093150]
  63. Nat Neurosci. 2005 Dec;8(12):1704-11 [PMID: 16286932]
  64. Neuroimage. 2011 Oct 1;58(3):955-62 [PMID: 21757014]
  65. Proc Natl Acad Sci U S A. 2013 Jun 25;110(26):E2428-36 [PMID: 23754384]
  66. J Trauma Stress. 2013 Oct;26(5):537-47 [PMID: 24151000]
  67. J Cogn Neurosci. 2000;12 Suppl 2:15-23 [PMID: 11506644]
  68. Hum Brain Mapp. 2001 Nov;14(3):140-51 [PMID: 11559959]
  69. Biol Psychiatry. 2018 Jul 15;84(2):129-137 [PMID: 29246436]
  70. Trends Cogn Sci. 2015 Feb;19(2):73-7 [PMID: 25577706]
  71. Brain. 2014 Jan;137(Pt 1):12-32 [PMID: 23869106]
  72. Acta Psychiatr Scand. 2005 Apr;111(4):291-9 [PMID: 15740465]

Grants

  1. R01 MH119132/NIMH NIH HHS
  2. R21 MH108753/NIMH NIH HHS
  3. T32 DA022981/NIDA NIH HHS

MeSH Term

Extinction, Psychological
Fear
Female
Humans
Magnetic Resonance Imaging
Male
Reinforcement, Psychology
Stress Disorders, Post-Traumatic

Word Cloud

Created with Highcharts 10.0.0fearPTSDRLmodel-basedprocessesextinctionlearningacquisitionimpairedconditioningmodelwithinestimationposttraumaticstressdisorderComputationalmodelsmodel-freedisruptedamongidentifywhetherevidencewomenSCRprovideResultsreducedactivityupdatingpredictedsymptomsgreatervalueencodingmayresponseFearLearningtheoriespurportfear-learningsupportdesignedcapturespecificinvolvedprimarilyassessedtrial-and-errorreinforcementAlthoughpreviousstudiesindicatedaspectsindividualsresearchyetinferentialcontextuallydrivenGivenempiricalaberrantcontextualmodulationpresentstudysoughtalteredinterpersonalviolenceIPV-relatedn=85usingcomputationalmodelingModel-freehybridappliedskinconductanceresponsescollectedfoundbestfitdataParameterscarriedforwardneuroimaginganalysesvoxel-wiseindependentcomponentanalysisrevealedvisualprocessingregionsuniquelyhigherAdditionallycontrollingleftfrontoparietalnetworkdorsomedialprefrontalcortexassault-relatedcontributesafetyfurthermorerelatetreatmentegpoorerexposuretherapyValuelatent-stateupdate-relatedneuralpredictsymptomseverityNeuroimagingReinforcement

Similar Articles

Cited By